Independent evolution of functional MHC class II DRB genes in New World bat species

Schad, Julia; Voigt, Christian C.; Greiner, Sabine; Dechmann, Dina K. N.; Sommer, Simone

doi:10.1007/s00251-012-0609-1

Cited by 18 publications

(46 citation statements)

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“…These genes are affected by pathogen-mediated selection in a wide range of vertebrate species (Wegner et al 2003;Piertney and Oliver 2006;Savage and Zamudio 2011), and spatial patterns of variation in the MHC can serve as an immunogenetic proxy for the potential of a declining population to adapt to shifting selection by pathogens (Hawley and Fleischer 2012;Kyle et al 2014). The MHC has been studied in several bats, including a suite of Neotropical phyllostomid species (Schad et al 2012b;Real-Monroy et al 2014;Salmier et al 2016), the sac-winged bat (Saccopteryx bilineata; Mayer and Brunner 2007), and two North American Myotis species (M. velifer, M. velesi;Richman et al 2010). MHC variants are correlated with ectoparasite load in the lesser bulldog bat (Noctilio albiventris; Schad et al 2012a).…”

Section: Introductionmentioning

confidence: 99%

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

Davy

Donaldson

Rico

et al. 2017

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The fungus that causes bat white-nose syndrome (WNS) recently leaped from eastern North America to the Pacific Coast. The pathogen's spread is associated with the genetic population structure of a host (Myotis lucifugus). To understand the fine-scale neutral and immunogenetic variation among northern populations of M. lucifugus, we sampled 1142 individuals across the species' northern range. We used genotypes at 11 microsatellite loci to reveal the genetic structure of, and directional gene flow among, populations to predict the likely future spread of the pathogen in the northwest and to estimate effective population size (N e ). We also pyrosequenced the DRB1-like exon 2 of the class II major histocompatibility complex (MHC) in 160 individuals to explore immunogenetic selection by WNS. We identified three major neutral genetic clusters: Eastern, Montane Cordillera (and adjacent sampling areas), and Haida Gwaii, with admixture at intermediate areas and significant substructure west of the prairies. Estimates of N e were unexpectedly low (289-16 000). Haida Gwaii may provide temporary refuge from WNS, but the western mountain ranges are not barriers to its dispersal in M. lucifugus and are unlikely to slow its spread. Our major histocompatibility complex (MHC) data suggest potential selection by WNS on the MHC, but gene duplication limited the immunogenetic analyses.

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Section: Introductionmentioning

confidence: 99%

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

Davy

Donaldson

Rico

et al. 2017

FACETS

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“…As proposed by [57], the nomenclature of MHC alleles for non-human species was used: to each allele a prefix (the first two letters of the genus and the species names) was given, with the serial number attached as follows: Cape - DRB for C. perspicillata , Dero - DRB for D. rotundus and Momo-DRB for M. molossus. Cape - DRB alleles identified in this study were named after the 15 alleles previously described by [35]. …”

Section: Methodsmentioning

confidence: 99%

“…, Noctilio spp . and Carollia perspicillata [35]. Other studies, investigating the diversity of MHC DRB , showed significant differences in the polymorphism of MHC genes between species.…”

Section: Introductionmentioning

confidence: 99%

“…Other studies, investigating the diversity of MHC DRB , showed significant differences in the polymorphism of MHC genes between species. This polymorphism was essentially influenced by (1) a pathogen-driven selection [36], (2) a social structure driven by MHC-mediated post-copulatory mechanisms [37], (3) diversifying selection and recombination events [35, 38] and (4) geographical constraints resulting in spatial variation of pathogen-mediated selection and enhanced susceptibility to environmental changes [39, 40]. …”

Section: Introductionmentioning

confidence: 99%

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Spatial pattern of genetic diversity and selection in the MHC class II DRB of three Neotropical bat species

et al. 2016

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BackgroundAlthough bats are natural reservoirs of many pathogens, few studies have been conducted on the genetic variation and detection of selection in major histocompatibility complex (MHC) genes. These genes are critical for resistance and susceptibility to diseases, and host–pathogen interactions are major determinants of their extensive polymorphism. Here we examined spatial patterns of diversity of the expressed MHC class II DRB gene of three sympatric Neotropical bats, Carollia perspicillata and Desmodus rotundus (Phyllostomidae), and Molossus molossus (Molossidae), all of which use the same environments (e.g., forests, edge habitats, urban areas). Comparison with neutral marker (mtDNA D-loop) diversity was performed at the same time.ResultsTwenty-three DRB alleles were identified in 19 C. perspicillata, 30 alleles in 35 D. rotundus and 20 alleles in 28 M. molossus. The occurrence of multiple DRB loci was found for the two Phyllostomidae species. The DRB polymorphism was high in all sampling sites and different signatures of positive selection were detected depending on the environment. The patterns of DRB diversity were similar to those of neutral markers for C. perspicillata and M. molossus. In contrast, these patterns were different for D. rotundus for which a geographical structure was highlighted. A heterozygote advantage was also identified for this species. No recombination or gene conversion event was found and phylogenetic relationships showed a trans-species mode of evolution in the Phyllostomids.ConclusionsThis study of MHC diversity demonstrated the strength of the environment and contrasting pathogen pressures in shaping DRB diversity. Differences between positively selected sites identified in bat species highlighted the potential role of gut microbiota in shaping immune responses. Furthermore, multiple geographic origins and/or population admixtures observed in C. perspicillata and M. molossus populations acted as an additional force in shaping DRB diversity. In contrast, DRB diversity of D. rotundus was shaped by environment rather than demographic history.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0802-1) contains supplementary material, which is available to authorized users.

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“…However, these predicted sites were strongly and significantly correlated with the 15 peptide-binding region residues determined based on protein crystallography (Pearson's correlation ranged from r(29) ¼ 0.49, p , 0.01, primates, to r(12) ¼ 0.93, p , 0.001, rodents). In addition, these 15 sites are known to be involved with antigen binding and have been shown to be under positive selection across a diverse set of taxa (carnivores, rodents and primates [41]; bats [42]). Therefore, we focus analyses on these documented 15 ABS sites, though analyses with putative taxonspecific ABS sites show overall consistent results (see the electronic supplementary material, figure S3).…”

Section: Materials and Methods (A) Major Histocompatibility Complex Datamentioning

confidence: 99%

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

et al. 2013

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Understanding drivers of genetic diversity at the major histocompatibility complex (MHC) is vitally important for predicting how vertebrate immune defence might respond to future selection pressures and for preserving immunogenetic diversity in declining populations. Parasite-mediated selection is believed to be the major selective force generating MHC polymorphism, and while MHC-based mating preferences also exist for multiple species including humans, the general importance of mate choice is debated. To investigate the contributions of parasitism and sexual selection in explaining among-species variation in MHC diversity, we applied comparative methods and metaanalysis across 112 mammal species, including carnivores, bats, primates, rodents and ungulates. We tested whether MHC diversity increased with parasite richness and relative testes size (as an indicator of the potential for mate choice), while controlling for phylogenetic autocorrelation, neutral mutation rate and confounding ecological variables. We found that MHC nucleotide diversity increased with parasite richness for bats and ungulates but decreased with parasite richness for carnivores. By contrast, nucleotide diversity increased with relative testes size for all taxa. This study provides support for both parasite-mediated and sexual selection in shaping functional MHC polymorphism across mammals, and importantly, suggests that sexual selection could have a more general role than previously thought.

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Independent evolution of functional MHC class II DRB genes in New World bat species

Cited by 18 publications

References 80 publications

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

Spatial pattern of genetic diversity and selection in the MHC class II DRB of three Neotropical bat species

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

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